Atypically high influence of subcortical activity on primary sensory regions in autism

Luigi Lorenzini; Guido van Wingen; Leonardo Cerliani

doi:10.1016/j.nicl.2021.102839

Atypically high influence of subcortical activity on primary sensory regions in autism

Neuroimage Clin. 2021:32:102839. doi: 10.1016/j.nicl.2021.102839. Epub 2021 Oct 5.

Authors

Luigi Lorenzini¹, Guido van Wingen², Leonardo Cerliani³

Affiliations

¹ Dept. of Psychiatry, Amsterdam UMC, University of Amsterdam, Amsterdam Neuroscience, Meibergdreef 5, 1105AZ Amsterdam, The Netherlands; Dept. Radiology and Nuclear Medicine, Amsterdam UMC, VU University, Amsterdam Neuroscience, De Boelelaan 1117, 1081HV Amsterdam, The Netherlands. Electronic address: l.lorenzini@amsterdamumc.nl.
² Dept. of Psychiatry, Amsterdam UMC, University of Amsterdam, Amsterdam Neuroscience, Meibergdreef 5, 1105AZ Amsterdam, The Netherlands; Amsterdam Brain and Cognition, University of Amsterdam, Nieuwe Achtergracht 129-B, 1018WT, University of Amsterdam, The Netherlands.
³ Dept. of Psychiatry, Amsterdam UMC, University of Amsterdam, Amsterdam Neuroscience, Meibergdreef 5, 1105AZ Amsterdam, The Netherlands; Amsterdam Brain and Cognition, University of Amsterdam, Nieuwe Achtergracht 129-B, 1018WT, University of Amsterdam, The Netherlands; Netherlands Institute for Neuroscience, Social Brain Lab, Meibergdreef 47, 1105BA Amsterdam, The Netherlands.

Abstract

Background: Hypersensitivity, stereotyped behaviors and attentional problems in autism spectrum disorder (ASD) are compatible with inefficient filtering of undesired or irrelevant sensory information at early stages of neural processing. This could stem from the persistent overconnectivity between primary sensory regions and deep brain nuclei in both children and adults with ASD - as reported by several previous studies - which could reflect a decreased or arrested maturation of brain connectivity. However, it has not yet been investigated whether this overconnectivity can be modelled as an excessive directional influence of subcortical brain activity on primary sensory cortical regions in ASD, with respect to age-matched typically developing (TD) individuals.

Methods: To this aim, we used dynamic causal modelling to estimate (1) the directional influence of subcortical activity on cortical processing and (2) the functional segregation of primary sensory cortical regions from subcortical activity in 166 participants with ASD and 193 TD participants from the Autism Brain Imaging Data Exchange (ABIDE). We then specifically tested the hypothesis that the age-related changes of these indicators of brain connectivity would differ between the two groups.

Results: We found that in TD participants age was significantly associated with decreased influence of subcortical activity on cortical processing, paralleled by an increased functional segregation of cortical sensory processing from subcortical activity. Instead these effects were highly reduced and mostly absent in ASD participants, suggesting a delayed or arrested development of the segregation between subcortical and cortical sensory processing in ASD.

Conclusion: This atypical configuration of subcortico-cortical connectivity in ASD can result in an excessive amount of unprocessed sensory input relayed to the cortex, which is likely to impact cognitive functioning in everyday situations where it is beneficial to limit the influence of basic sensory information on cognitive processing, such as activities requiring focused attention or social interactions.

Keywords: Autism Spectrum Disorder; Brain Connectivity; Brain maturation; Dynamic Causal Modelling; Primary sensory cortex; Subcortical nuclei.

Publication types

Research Support, Non-U.S. Gov't

MeSH terms

Attention
Autism Spectrum Disorder* / diagnostic imaging
Autistic Disorder*
Brain / diagnostic imaging
Brain Mapping
Humans
Magnetic Resonance Imaging